Assessment of listing and categorisation of animal diseases within the framework of the Animal Health Law (Regulation (EU)2016/429): Infection with salmonid alphavirus (SAV)

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ADOPTED: 27 September 2023 doi: 10.2903/j.efsa.2023.8327

Assessment of listing and categorisation of animal diseases within the framework of the Animal Health Law (Regulation

(EU)2016/429): Infection with salmonid alphavirus (SAV)

EFSA Panel on Animal Health and Welfare (AHAW),

Søren Saxmose Nielsen, Julio Alvarez, Paolo Calistri, Elisabetta Canali, Julian Ashley Drewe, Bruno Garin-Bastuji, Jose Luis Gonzales Rojas, Christian Gortazar, Mette S. Herskin, Virginie Michel, MiguelAngel Miranda Chueca, Barbara Padalino, Helen Clare Roberts, Hans Spoolder, Karl Stahl, Antonio Velarde, Arvo Viltrop, Christoph Winckler, James Bron, Niels Jorgen Olesen, Hilde Sindre, David Stone, Niccolo Vendramin, Sotiria Eleni Antoniou,

Alessandro Broglia, Anna Eleonora Karagianni, Alexandra Papanikolaou and Dominique Joseph Bicout

Abstract

Infection with salmonid alphavirus (SAV) was assessed according to the criteria of the Animal Health Law (AHL), in particular the criteria of Article 7 on disease profile and impacts, Article 5 on its eligibility to be listed, Annex IV for its categorisation according to disease prevention and control rules as laid out in Article 9 and Article 8 for listing animal species related to infection with SAV. The assessment was performed following the ad hoc method on data collection and assessment developed by AHAW Panel and already published. The outcome reported is the median of the probability ranges provided by the experts, which indicates whether each criterion is fulfilled (lower bound ≥ 66%) or not (upper bound ≤33%), or whether there is uncertainty about fulfilment. Reasoning points are reported for criteria with an uncertain outcome. According to the assessment, it was uncertain whether infection with salmonid alphavirus can be considered eligible to be listed for Union intervention according to Article 5 of the AHL (50–80% probability). According to the criteria in Annex IV, for the purpose of categorisation related to the level of prevention and control as in Article 9 of the AHL, the AHAW Panel concluded that infection with salmonid alphavirus does not meet the criteria in Section 1 (Category A;

5–10% probability of meeting the criteria) and it is uncertain whether it meets the criteria in Sections 2, 3, 4 and 5 (Categories B, C, D and E; 50–90%, probability of meeting the criteria). The animal species to be listed for infection with SAV according to Article 8 criteria are provided.

Keywords: aquatic animals, animal health law, salmonid alphavirus, listing, categorisation, impact

Requestor:European Commission Question number:EFSA-Q-2023-00065 Correspondence: [email protected]

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Panel members: Søren Saxmose Nielsen, Julio Alvarez, Dominique Joseph Bicout, Paolo Calistri, Elisabetta Canali, Julian Ashley Drewe, Bruno Garin-Bastuji, Jose Luis Gonzales Rojas, Christian Gortazar, Mette S Herskin, Virginie Michel, MiguelAngel Miranda Chueca, Barbara Padalino, Helen Clare Roberts, Hans Spoolder, Karl Stahl, Antonio Velarde, Arvo Viltrop and Christoph Winckler.

Map Disclaimer: The designations employed and the presentation of material on any maps included in this scientiﬁc output do not imply the expression of any opinion whatsoever on the part of the European Food Safety Authority concerning the legal status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries.

Declarations of interest: If you wish to access the declaration of interests of any expert contributing to an EFSA scientiﬁc assessment, please [email protected].

Acknowledgements: The AHAW Panel wishes to acknowledge the expert Dr Estelle Meroc selected through the Individual Scientiﬁc Advisor schema (ISA expert; EOI/EFSA/SCIENCE/2022/01 – CT 05 BIOHAW contract) for conducting the literature review on the disease proﬁle and the parameters of the criteria of Article 7 of AHL and drafting the fact sheet.

Suggested citation: EFSA FEEDAP Panel (EFSA Panel on Animal Health and Welfare), Nielsen, S. S., Alvarez, J., Calistri, P., Canali, E., Drewe, J. A., Garin-Bastuji, B., Gonzales Rojas, J. L., Gortazar, C., Herskin, M. S., Michel, V., Miranda Chueca, M. A., Padalino, B., Roberts, H. C., Spoolder, H., Stahl, K., Velarde, A., Viltrop, A., Winckler, C.,. . . Bicout, D. J. (2023). Assessment of listing and categorisation of animal diseases within the framework of the Animal Health Law (Regulation (EU)2016/429): Infection with salmonid alphavirus (SAV).EFSA Journal,21(10), 1–80.https://doi.org/10.2903/j.efsa.2023.8327 ISSN: 1831-4732

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Table of contents

Abstract... 1

1. Introduction... 5

1.1. Background and Terms of Reference as provided by the requestor... 5

1.1.1. Background... 5

1.1.2. Disease speciﬁc information... 5

1.1.3. Terms of Reference... 6

1.2. Interpretation of the Terms of Reference... 6

2. Data and methodologies... 7

3. Assessment... 8

3.1. Assessment according to article 7 criteria... 8

3.1.1. Article 7(a) disease proﬁle... 8

3.1.1.1. Article 7(a)(i) Animal species concerned by the disease... 8

3.1.1.2. Article 7(a)(ii) The morbidity and mortality rates of the disease in animal populations... 10

3.1.1.3. Article 7(a)(iii) The zoonotic character of the disease... 11

3.1.1.4. Article 7(a)(iv) The resistance to treatments, including antimicrobial resistance... 11

3.1.1.5. Article 7(a)(v) The persistence of the disease in an animal population or the environment... 11

3.1.1.6. Article 7(a)(vi) The routes and speed of transmission of the disease between animals, and, when relevant, between animals and humans... 12

3.1.1.7. Article 7(a)(vii) The absence or presence and distribution of the disease in the union, and, where the disease is not present in the union, the risk of its introduction into the union... 13

3.1.1.8. Article 7(a)(viii) The existence of diagnostic and disease control tools... 14

3.1.2. Article 7(b) The impact of disease... 15

3.1.2.1. Article 7(b)(i) The impact of the disease on agricultural and aquaculture production and other parts of the economy... 15

3.1.2.2. Article 7(b)(ii) The impact of the disease on human health... 15

3.1.2.3. Article 7(b)(iii) The impact of the disease on animal welfare... 16

3.1.2.4. Article 7(b)(iv) The impact of the disease on biodiversity and the environment... 16

3.1.3. Article 7(c) Its potential to generate a crisis situation and its potential use in bioterrorism... 17

3.1.4. Article 7(d) The feasibility, availability and effectiveness of the following disease prevention and control measures... 17

3.1.4.1. Article 7(d)(i) Diagnostic tools and capacities... 17

3.1.4.2. Article 7(d)(ii) vaccination... 18

3.1.4.3. Article 7(d)(iii) Medical treatments... 19

3.1.4.4. Article 7(d)(iv) Biosecurity measures... 20

3.1.4.5. Article 7(d)(v) Restrictions on the movement of animals and products... 20

3.1.4.6. Article 7(d)(vi) Killing of animals... 21

3.1.4.7. Article 7(d)(vii) Disposal of carcasses and other relevant animal by-products... 21

3.1.4.8. Article 7(d)(viii) Selective breeding; genetic resistance to infection... 22

3.1.5. Article 7(e) The impact of disease prevention and control measures... 23

3.1.5.1. Article 7(e)(i) The direct and indirect costs for the affected sectors and the economy as a whole... 23

3.1.5.2. Article 7(e)(ii) The societal acceptance of disease prevention and control measures... 23

3.1.5.3. Article 7(e)(iii) The welfare of affected subpopulations of kept and wild animals... 24

3.1.5.4. Article 7(e)(iv) The environment and biodiversity... 24

3.2. Assessment of infection with salmonid alphavirus according to Article 5 criteria of AHL on its eligibility to be listed... 25

3.2.1. Detailed outcome on Article 5 criteria... 25

3.2.2. Reasoning for uncertain outcome on Article 5 criteria... 26

3.2.3. Overall outcome on Article 5 criteria... 27

3.3. Assessment infection with Salmonid alphavirus according to criteria in Annex IV for the purpose of categorisation as in Article 9 of the AHL... 27

3.3.1. Detailed outcome on category a criteria... 27

3.3.1.1. Reasoning for uncertain outcome on category a criteria... 28

3.3.2. Detailed outcome on category B criteria... 30

3.3.2.1. Reasoning for uncertain outcome on Category B criteria... 31

3.3.3. Detailed outcome on Category C criteria... 31

3.3.3.1. Reasoning for uncertain outcome on category C criteria... 33

3.3.4. Detailed outcome on Category D criteria... 34

3.3.5. Detailed outcome on Category E criteria... 34

3.3.6. Overall outcome on criteria in Annex IV for the purpose of categorisation as in Article 9... 34

3.4. Assessment of infection with Salmonid alphavirus according to Article 8 criteria of the AHL... 36

4. Conclusions... 37

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References... 38 Abbreviations... 43 Appendix A–Expert's judgement plotted by question... 44

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1. Introduction

1.1. Background and Terms of Reference as provided by the requestor

1.1.1. Background

Article 5 of the Regulation (EU) 2016/429 of the European Parliament and of the Council on transmissible animal diseases (Animal Health Law [AHL]),¹provides for the list of diseases to which the rules set out in the AHL apply. These rules include the assessment provided for in Article 7 and the categorisation of those diseases as provided for in Article 9 of that Regulation.

In addition to the list of ﬁve signiﬁcant diseases laid down in Article 5(1) of the AHL, a further list of animal diseases is set out in Annex II to that Regulation, which may be amended by means of a delegated regulation.

In addition, there are other transmissible diseases of aquatic animals for which certain control or trade measures apply today in accordance with Article 226(3) of the AHL, and which are not included in Annex II to the AHL.

Details of those diseases and the Member States or parts thereof which are regarded as being free from one or more of them, or which are subject to an eradication programme, are set out in Annexes I and II to Commission Implementing Decision (EU) 2021/260². The aquatic species which are considered to be susceptible to those diseases are set out in Annex III to that Implementing Decision.

At least some of these diseases may fulﬁl the criteria to be listed in accordance with Article 5(3), following assessment in accordance with Article 7. In cases where listing is justiﬁed, these diseases should also be categorised in accordance with Article 9(1) and Annex IV of the AHL, and species, or groups of animal species, that are either susceptible to the diseases in question or have the capability to act as vectors, should be listed in accordance with Article 8(3) of the AHL.

The Commission, therefore, requires scientiﬁc advice concerning the following diseases, within the framework described above:

•

Spring viraemia of carp (SVC);

•

Bacterial kidney disease (BKD);

•

Infectious pancreatic necrosis (IPN);

•

Infection with Gyrodactylus salaris(GS);

•

Infection with salmonid alphavirus (SAV).

1.1.2. Disease speciﬁc information (a) Spring viraemia of carp (SVC)

Speciﬁc international trade standards for infection with spring viraemia of carp virus are provided for in Chapter 10.9. of WOAH (formerly OIE) Aquatic Animal Health Code (the WOAH [formerly OIE]

Code), as well as in Chapter 2.3.9 of the WOAH (formerly OIE) Manual of Diagnostic for Aquatic Animals (the WOAH [formerly OIE] Manual).

In the existing EU legislative acts, spring viraemia of carp is referred to in Commission Implementing Decision (EU) 2021/260 of 11 February 2021, approving national measures designed to limit the impact of certain diseases of aquatic animals in accordance with Article 226(3) of Regulation (EU) 2016/429 of the European Parliament and of the Council and repealing Commission Decision 2010/221/EU.

(b) Bacterial kidney disease (BKD)

Speciﬁc international trade standards for bacterial kidney disease are not provided in the Aquatic Animal Health Code (the WOAH [formerly OIE] Code) or in the WOAH (formerly OIE) Manual of Diagnostic for Aquatic Animals (the WOAH [formerly OIE] Manual].

Bacterial kidney disease is however, referred to in Commission Implementing Decision (EU) 2021/

260 of 11 February 2021, approving national measures designed to limit the impact of certain diseases

1Regulation (EU) 2016/429 of the European Parliament and of the Council of 9 March 2016 on transmissible animal diseases and amending and repealing certain acts in the area of animal health (‘Animal Health Law’). OJ L 84, 31.3.2016, p. 1.

2Commission Implementing Decision (EU) 2021/260 of 11 February 2021 approving national measures designed to limit the impact of certain diseases of aquatic animals in accordance with Article 226(3) of Regulation (EU) 2016/429 of the European Parliament and of the Council and repealing Commission Decision 2010/221/EU. OJ L 59, 19.2.2021, p. 1–9.

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of aquatic animals in accordance with Article 226(3) of Regulation (EU) 2016/429 of the European Parliament and of the Council and repealing Commission Decision 2010/221/EU.

(c) Infectious pancreatic necrosis (IPN)

Speciﬁc international trade standards for infectious pancreatic necrosis are not provided in the Aquatic Animal Health Code (the WOAH [formerly OIE] Code) or in the WOAH (formerly OIE) Manual of Diagnostic for Aquatic Animals (the WOAH [formerly OIE] Manual).

Infectious pancreatic necrosis is however, referred to in Commission Implementing Decision (EU) 2021/260 of 11 February 2021, approving national measures designed to limit the impact of certain diseases of aquatic animals in accordance with Article 226(3) of Regulation (EU) 2016/429 of the European Parliament and of the Council and repealing Commission Decision 2010/221/EU.

(d) Infection withGyrodactylus salaris(GS)

Speciﬁc international trade standards for infection with Gyrodactylus salaris are provided for in Chapter 10.3. of the WOAH (formerly OIE) Aquatic Animal Health Code (the WOAH [formerly OIE]

In the existing EU legislative acts, infection with Gyrodactylus salaris is referred to in Commission Implementing Decision (EU) 2021/260 of 11 February 2021, approving national measures designed to limit the impact of certain diseases of aquatic animals in accordance with Article 226(3) of Regulation (EU) 2016/429 of the European Parliament and of the Council and repealing Commission Decision 2010/221/EU.

(e) Infection with salmonid alphavirus (SAV)

Speciﬁc international trade standards for infection with salmonid alphavirus are provided for in Chapter 10.5. of the WOAH (formerly OIE) Aquatic Animal Health Code (the WOAH [formerly OIE]

In the existing EU legislative acts, salmonid alphavirus is referred to in Commission Implementing Decision (EU) 2021/260 of 11 February 2021, approving national measures designed to limit the impact of certain diseases of aquatic animals in accordance with Article 226(3) of Regulation (EU) 2016/429 of the European Parliament and of the Council and repealing Commission Decision 2010/

221/EU.

1.1.3. Terms of Reference

In view of the above, the Commission asks EFSA for a scientiﬁc opinion as follows:

1) for each of the diseases referred to above, an assessment, taking into account the criteria laid down in Article 7 of the AHL, on the eligibility of the disease to be listed for Union intervention as laid down in Article 5(3) of the AHL;

2) for each of the diseases mentioned above:

a) an assessment of its compliance with each of the criteria in Annex IV to the AHL for the purpose of categorisation of diseases in accordance with Article 9(1) of the AHL;

b) a list of animal species that should be considered candidates for listing in accordance with Article 8 of the AHL.

1.2. Interpretation of the Terms of Reference

The interpretation of the terms of reference (ToRs) is as in Section 1.2of the scientiﬁc opinion on the ad hoc method to be followed for the assessment on listing and categorisation of animal diseases within the AHL framework (EFSA AHAW Panel, 2017a).

The present document reports the results of the assessment on the infection with salmonid alphavirus (SAV) according to the criteria of the AHL articles as follows:

•

Article 7: infection with SAV proﬁle and impact;

•

Article 5: eligibility of infection with SAV to be listed;

•

Article 9: categorisation of infection with SAV according to disease prevention and control rules as in Annex IV. Each category foresees the application of certain disease prevention and

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control rules to the respective listed diseases when the disease in question fulﬁls the criteria laid down in the relevant Section of Annex IV of AHL (Sections 1–5 which correspond to Categories A–E, respectively):

Category A: listed diseases that do not normally occur in the Union and for which immediate eradication measures must be taken as soon as they are detected.

Category B: listed diseases, which must be controlled in all Member States with the goal of eradicating them throughout the Union.

Category C: listed diseases which are of relevance to some Member States and for which measures are needed to prevent them from spreading to parts of the Union that are ofﬁcially disease-free or that have eradication programmes for the listed disease concerned.

Category D: listed diseases for which measures are needed to prevent them from spreading on account of their entry into the Union or movements between Member States.

Category E: listed diseases for which there is a need for surveillance within the Union;

•

Article 8: list of animal species related to infection with SAV.

2. Data and methodologies

In order to address the ToRs as provided by the Commission, regarding the listing and categorisation of animal diseases within the framework of AHL, the EFSA AHAW Panel has developed an ad hoc methodology for the data collection and the assessment (EFSA AHAW Panel, 2017a). This ad hoc methodology has been used for assessing any animal disease in a uniform and consistent way and is the one used also for the current Scientiﬁc Opinion and constitutes the Protocol of the Assessment.

For the needs of the listing and categorisation of aquatic animal diseases, the following deviations in Sections 2.1.2 and 2.3.1 of the ad hoc methodology (EFSA AHAW Panel, 2017a) were considered necessary for the assessment:

a) An EFSA working group (WG) of experts with expertise in aquatic animal diseases was established to support the assessment of the EFSA AHAW panel.

b) Section 2.1.2: The fact sheet on the disease proﬁle and on the parameters of the criteria and of Article 7 of AHL has been outsourced not only to experts with disease-speciﬁc expertise but also to experts with expertise in veterinary epidemiology or in aquatic animal diseases.

The fact sheet was reviewed by the EFSA WG of experts and the comments provided were addressed by the contractor.

c) Section 2.3.1: In addition to AHAW Panel experts as foreseen in the methodology (EFSA AHAW Panel, 2017a), ﬁve experts from the EFSA WG with expertise in aquatic animal diseases participated in the judgement.

The following assessment was performed by the EFSA Panel on Animal Health and Welfare (AHAW) based on the information collected and compiled in the form of a fact sheet as in Section 3.1of the present document. The outcome is the median of the probability ranges provided by the experts, which are accompanied by verbal interpretations only when they fall within the ranges as spelt out in Table 1.

Table 1: Approximate probability scale recommended for harmonised use in EFSA (EFSA Scientiﬁc Committee, 2018)

Probability term Subjective probability range

Almost certain 99–100%

Extremely likely 95–99%

Very likely 90–95%

Likely 66–90%

About as likely as not 33–66%

Unlikely 10–33%

Very unlikely 5–10%

Extremely unlikely 1–5%

Almost impossible 0–1%

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Section 3.1 below includes the information of the fact sheet on the disease proﬁle and the parameters of the criteria of Article 7 of AHL and has been drafted by the selected expert through the Individual Scientiﬁc Advisor schema (ISA expert; EOI/EFSA/SCIENCE/2022/01 – CT 05 BIOHAW contract) and reviewed by the EFSA working group of experts.

3. Assessment

3.1. Assessment according to article 7 criteria

This Section presents the assessment of infection with SAV according to the criteria of Article 7 of the AHL and the related parameters in Table 2 of the Scientific Opinion on ad hoc methodology (EFSA AHAW Panel, 2017a). The assessment is based on the information contained in the fact sheet on the disease profile and the parameters of the criteria of Article 7 of AHL (see Section 2.1 of the Scientific Opinion on the ad hoc methodology).

3.1.1. Article 7(a) disease proﬁle

Salmonid alphavirus is a single-stranded RNA virus, which belongs to the genusAlphaviruswithin the family Togaviridae, and is a pathogen of salmonid aquaculture (Snow et al., 2010). So far, seven genotypes of SAV (SAV1–7) have been identiﬁed based on sequence analysis: SAV1,3,4,5,6 typically cause pancreas disease (PD) in seawater Atlantic salmon (Salmo salar). SAV2 is divided into two variants:

the freshwater variant (SAV2 FW) which is responsible for sleeping disease (SD) in freshwater rainbow trout (Oncorhynchus mykiss) and the marine variant (SAV2 MW) which causes PD and has been isolated from diseased Atlantic salmon in Scotland and Norway. The seventh genotype has been detected in ballan wrasse (Labrus bergylta) but has not been shown to cause PD in salmonids so far (Tighe et al., 2020). These genotypes all belong to the same virus species, abbreviated as salmon pancreas disease virus (SPDV) by the International Committee on Taxonomy of Viruses (ICTV) (Chen et al., 2018).

The primary target organs for SAV are the heart and the pancreas, and it is considered likely that ﬁsh become infected through the gills, skin and intestine (Jansen et al., 2017). Clinical signs associated with PD include sudden inappetence, lethargy and an increased number of faecal casts in the cages, as well as mortality. SD is an infectious disease similar to PD, which represents an increasing problem throughout Europe, causing high mortality and growth retardation of ﬁsh (Graham et al., 2007a; McLoughlin and Graham, 2007; Deperasinska et al., 2018). Lesions of PD and SD include necrosis of the pancreatic tissue as well as alterations in the heart and the skeletal muscle. In 2014, SAV was listed by the World Organisation for Animal Health (WOAH) (WOAH, 2021; Baumgartner et al., 2022).

3.1.1.1. Article 7(a)(i) Animal species concerned by the disease Susceptible animal species

Note: Farmed and wild aquatic animals cannot be easily distinguished.

Parameter 1– Naturally susceptible wildlife species (or family/orders)

The species naturally susceptible to SAV are listed in Table2. Atlantic salmon and rainbow trout are the species with the highest likelihood of infection with SAV, and ﬁsh in all life stages are susceptible.

Additionally, species for which there is incomplete evidence for susceptibility according to the WOAH include long rough dab (Hippoglossoides platessoides), plaice (Pleuronectes platessa) and ballan wrasse (Labrus bergylta) (WOAH, 2021).

Table 2: Naturally susceptibleﬁsh species Fish species (Scientiﬁc

Name) Genotype Reference

Arctic charr (Salvelinus alpinus) SAV2 Lewisch et al. (2018), World Organisation for Animal Health (2022b)

Atlantic salmon (Salmo salar) SAV1-2-3-4-5-6 WOAH (2022a,b)

Common dab (Limanda limanda) SAV5 Snow et al. (2010), Andersen and Blindheim (2022), World Organisation for Animal Health (2022b)

Rainbow trout (Oncorhynchus mykiss)

SAV1-2-3 Fringuelli et al. (2008), WOAH (2022a,b)

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Parameter 2– Naturally susceptible domestic/farmed species (or family/orders)

The species naturally susceptible to SAV are listed in Table2. Atlantic salmon and rainbow trout are the species with the highest likelihood of infection with SAV, and all life stages are susceptible.

Parameter 3– Experimentally susceptible wildlife species (or family/orders)

Wildﬁsh species that were found to be experimentally susceptible to SAV and that are not already mentioned in the list of naturally susceptibleﬁsh species in Table2are reported in Table3.

Parameter 4– Experimentally susceptible domestic/farmed species (or family/orders)

Domestic/farmedﬁsh species that were found to be experimentally susceptible to SAV and that are not already mentioned in the list of naturally susceptible ﬁsh species in Table2are reported in Table3.

Reservoir animal species

Parameter 5–Wild reservoir species (or family/orders)

The presence of SAV has been detected by RT-PCR in several species of pleuronectids through survey studies conducted in Ireland and Scotland; SAV RNA was retrieved in heart tissue from common dab (Table 2), European plaice and long rough dab (Snow et al., 2010; Bruno et al., 2014;

McCleary et al., 2014; Simons et al., 2016). However, the results of an experimental challenge trial conducted by Andersen and Blindheim (2022) indicated that pleuronectids carrying SAV do not transmit the virus to salmon. Recently, SAV was isolated from a pooled sample of asymptomatic ballan wrasse caught in Ireland (Ruane et al., 2018).

The WOAH has also reported that SAV has been detected by RT-PCR in tissues from the followingfish species with no sign of active infection: herring (Clupea harengus), longhorn sculpin (Myoxocephalus octodecemspinosus), haddock (Melanogrammus aeglefinus), Norway pout (Trisopterus esmarkii), saithe (Pollachius virens), whiting (Merlangius merlangus), Atlantic cod (Gadus morhua), Argentine hake (Merluccius hubbsi), European flounder (Platichthys flesus) and brown trout (Salmo trutta) (WOAH, 2021). In addition, SAV-neutralising antibodies have been detected in the serum of saithe (Gadus virens) sampled from Atlantic salmon cages with SAV-infectedfish (Graham et al., 2006).

Additionally, species for which there is incomplete evidence for susceptibility according to the WOAH include long rough dab (Hippoglossoides platessoides), plaice (Pleuronectes platessa) and ballan wrasse (Labrus bergylta) (WOAH, 2021).

Parameter 6– Domestic/farmed reservoir species (or family/orders)

There is evidence suggesting that some susceptible species that survive outbreaks will become long-term carriers of the virus (Graham et al., 2010), and, in consequence, farmed Atlantic salmon and rainbow trout can be considered the main reservoir species of SAV (Taksdal and Sindre, 2016). In addition, some of the wild reservoir species mentioned in Parameter 5 may also be farmed, for instance Atlantic cod (Gadus morhua) and ballan wrasse (Labrus bergylta) and could be possible reservoirs.

Vector animal species

Parameter 7–Wild vector species (or family/orders)

Unlike other alphaviruses, which typically require an arthropod vector to complete their life cycle, SAV is known to be transmitted directly from one primary host to another host (McLoughlin et al., 1996). However, Petterson et al. (2009) reported the presence of SAV3 RNA in salmon sea louse (Lepeophtheirus salmonis) in Norway. Nonetheless, active replication in the lice has not been demonstrated nor has it been possible to infect L. salmonis in the laboratory (Karlsen et al., 2015;

Karlsen and Johansen, 2017).

Parameter 8– Domestic/farmed vector species (or family/orders) No domestic/farmed species have been identiﬁed as vectors of SAV.

Table 3: Experimentally susceptibleﬁsh species

Fish species Genotype Experiment setting Reference

Brown trout (Salmo trutta) Not reported Infected intra-peritoneally Boucher et al. (1995)

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3.1.1.2. Article 7(a)(ii) The morbidity and mortality rates of the disease in animal populations

Morbidity

Parameter 1– Prevalence or incidence

The prevalence during SAV outbreaks in farmed Atlantic salmon is variable but usually high (> 70%). The prevalence in wild ﬁsh is largely unknown (WOAH, 2021). A few examples of (sero-) prevalence and incidence estimates are described in Table 4.

Parameter 2– Case-morbidity rate (% of infected animals that show clinical disease)

Graham et al. (2006) conducted a prospective longitudinal study of SAV infections in farmed Atlantic salmon and described cases of subclinical infection (Graham et al., 2006). A Norwegian ﬁeld study detected SAV-RNA in ﬁsh up to 71 weeks prior to the outbreak of clinical disease at the site (Jansen et al., 2010a). Aldrin et al. (2015) reported that up to one-third of SAV-infected salmon populations do not develop clinical PD. In Norway, infections with marine SAV2 are reported to generate a higher proportion of subclinical cases than SAV3 infections (Jansen et al., 2015, 2017).

Differences in susceptibility between salmon families have also been reported (McLoughlin et al., 2006).

Table 4: Measures of SAV prevalence and incidence in wild and farmedﬁsh Country Time

period Indicator Study

population Value Reference

Ireland 2006–2008 Within-farm prevalence

Farmed Atlantic salmon

Range: 80–100% Graham et al. (2010) Within-farm

seroprevalence

Range: 63–90%

Ireland 1990–2007 Yearly farm-level incidence rate

Range: 59% (2002) to 91% (2007)

McLoughlin et al. (2003), Ruane et al. (2008) Norway 2013–2021 Yearly farm-level

incidence

100 farms (2013 and 2021)

Sommerset et al. (2022) Rainbow trout 176 farms (2017)

Norway 2012 Animal-level prevalence

Wild Atlantic salmon

<0.89% Madhun et al. (2018) Norway 2008–2011 Yearly farm-level

incidence

Range: 75 farms (2009)-105 farms (2008)

Bang Jensen et al. (2012) Rainbow trout

Norway 2006–2008 Farm-level prevalence

63.9% (95% CI: 46.2–

78.7)

Jansen et al. (2010a) Norway 1998–2007 Yearly farm-level

incidence

Range: 7 farms (1998) 98 farms (2007)

Ruane et al. (2008) Norway 1996–2004 Animal-level

seroprevalence

Farmed Atlantic salmon and rainbow trout

70% Taksdal et al. (2007)

Animal-level prevalence

90%

UK 2004 Animal-level

seroprevalence

Farmed rainbow trout

29% Graham et al. (2007b)

Animal-level prevalence

58%

UK 2002 Within-farm

seroprevalence

90%–100% Graham et al. (2005) UK

(Scotland)

2006–2007 Farm-level prevalence

16% Lester et al. (2011)

25%

PD: Pancreas disease; SAV: Salmonid alphavirus; UK: United Kingdom.

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Parameter 3– Case-fatality rate (% of infected animals that die from the disease)

The cumulative mortality of PD at the farm level varies widely from very low to over 50% in severe cases (Graham et al., 2003). For instance, in Ireland, annual mortality from 2000 to 2010 ranged between 14% and 18%, reaching 40% in badly affected cages (McCleary et al., 2014). Examples of farm-level mortality estimates obtained duringﬁeld outbreaks are described in the following Table5.

3.1.1.3. Article 7(a)(iii) The zoonotic character of the disease Presence

Parameter 1– Report of zoonotic human cases (anywhere)

There is no evidence in the literature indicating that SAV can infect humans.

3.1.1.4. Article 7(a)(iv) The resistance to treatments, including antimicrobial resistance

Parameter 1– Resistant strain to any treatment; even at laboratory level Not applicable. No effective treatment for SAV is currently available.

3.1.1.5. Article 7(a)(v) The persistence of the disease in an animal population or the environment

Animal population

Parameter 1– Duration of infectious period in animals

In order to study PD transmission dynamics among salmon farms in Norway, Stene et al. (2014b) assumed that the infectious period lasted until the infected cohort was harvested. Indeed, a previous prospective longitudinal study observed that once SAV RNA was detected by RT-PCR at a site, it was persistently found until the end of the study period, up to 19 months after the ﬁrst detection (Jansen et al., 2010b).

Table 5: Mortality estimates observed duringﬁeld outbreaks in European countries Country Study

period Indicator Study population

Values (n = number of

estimates) Reference

Ireland 2006–2008 PD-related mortality

(n = 2): 10.9% and 30% Graham et al. (2010) Ireland 2003–2004 PD-related

mortality

Mean (n = 13): 18.8%

(range: 2–27%)

Rodger and Mitchell (2007) Ireland 2001–2003 PD-related

mortality

Mean (n = 13): 12%

(range: 1–42%)

McLoughlin et al. (2003) Ireland 1990–2007 PD-related

mortality

Range of yearly means (n: each year between 59% and 91% of Irish marine salmon sites): 4%

(1993)–23% (2007)

Crockford et al. (1999), McLoughlin et al. (2003), Ruane et al. (2008)

Norway 2003–2007 PD-related mortality

Farmed salmonids

Mean range (n = 150):

4% (2006), 11% (2003)

Stormoen et al. (2013) Norway 2007–2009 PD-related

cumulative mortality

Mean (n = 52): 22.6%

(SD = 13.2)

Bang Jensen et al. (2012)

Mean (n = 20): 6.9%

(range: 0.7–26.9%)

Jansen et al. (2010a) Norway 1996–2004 PD-related

mortality

Farmed Atlantic salmon and rainbow trout

Range (n = 31): 3–20% Taksdal et al. (2007)

Mean (n = 28): 21.6%

(range: 6.1–68.6%)

Stene et al. (2014a) Switzerland 2013 SD-related

mortality

Range (n = 3): 2–8% Schmidt-Posthaus et al.

(2014) n: number of outbreaks.

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In a cohabitant trial conducted in Atlantic salmon, the testing of faeces from the SAV genotypes 1, 3 and 6 challenge groups found positive results in each group, beginning at 1–3 weeks post-challenge (wpc) and remaining detectable for a further 2–3 weeks. Parallel testing of mucus samples found these positive at 2–3 wpc and they remained positive for a further 1–3 weeks (Graham et al., 2011).

In the context of a prospective longitudinal study of SAV infection in farmed Atlantic salmon, which aimed to gain a better understanding of the epidemiology of a natural outbreak of PD, the first evidence of infection was detected on day 146 when four of 20 fish were found to be viraemic by inoculating sera onto chinook salmon embryo-214 cells and staining after 3 days, and 1 out of 20 to be antibody positive. At the following sampling on day 153, only two of 20 fish were viraemic and 1 antibody positive. At the next sampling (day 158), no viraemic or antibody positive fish were detected.

However, throughout the study period, there were no clinical signs of PD and no signiﬁcant mortality attributed to PD (Graham et al., 2006).

Parameter 2– Presence and duration of latent infection period

Desvignes et al. (2002) detected SAV by 2 days post-challenge in all experimentally infected Atlantic salmon parr, and the peak value of viraemia was reached 4 days after the challenge.

Based on analyses of antibody production during cohabitation trials, the incubation period of PD has been estimated to be 7–10 days at a water temperature of 12–15°C (McLoughlin and Graham, 2007). From ﬁeld data, survival analysis demonstrated that cohorts exposed to the virus at decreasing sea temperature had a signiﬁcantly longer incubation period than cohorts infected when the sea temperature was increasing (Stene et al., 2014a).

Parameter 3– Presence and duration of the pathogen in healthy carriers

Prolonged persistence of a positive PCR signal by real-time RT-PCR can be found in infected populations, with the majority of populations remaining PCR positive until slaughter even when infected early during the seawater phase (Graham et al., 2010; Jansen et al., 2010a; Jansen et al., 2017). SAV has been grown in cell culture from tissues of infected ﬁsh at least 4–6 months after the initial SAV detection at a site (Jansen et al., 2010b).

Environment

Parameter 4 – Length of survival (days post-inoculation) of the agent and/or detection of DNA in selected matrices (soil, water, air) from the environment (scenarios: high and low temperature)

SAV has re-emerged at some farms following restocking, and the persistence of the virus in sediments may serve as a source of infection (Jones et al., 2015). SAV can remain infectious under experimental conditions for a long period in sterile seawater (McLoughlin and Graham, 2007). Testing was conducted under sterile conditions in seawater, half-strength seawater and fresh (hard) water, both in the absence and presence of added organic matter. SAV survival was shown to be inversely related to temperature and to be reduced by the presence of organic matter, with half-lives ranging from 1.5 to 61 days (Graham et al., 2007c). Skjold (2014) observed that SAV survive less than 72 hours in the natural environment, given a seawater temperature of around 10°C.

3.1.1.6. Article 7(a)(vi) The routes and speed of transmission of the disease between animals, and, when relevant, between animals and humans

Routes of transmission

Parameter 1–Types of routes of transmission from animal to animal (horizontal, vertical)

The main transmission route of SAV appears to be horizontal and via water contact. This has been supported by both experimental trials and ﬁeld observations (Deperasinska et al., 2018; WOAH, 2021).

Virus excretion is believed to be through natural excretion/secretion, which is supported by the detection of SAV-RNA in faeces and mucus from SAV-infected ﬁsh, as well as in the lipid surface layer around SAV-infected cages (Graham et al., 2012; Stene et al., 2016; Jansen et al., 2017).

The Norwegian Scientiﬁc Committee for Food Safety carried out a risk assessment and concluded that the risk of vertical transmission of SAV is negligible (Rimstad et al., 1991; Jansen et al., 2017;

WOAH, 2021).

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Parameter 2 –Types of routes of transmission between animals and humans (direct, indirect, including foodborne)

There is no evidence of SAV transmission between animals and humans.

Speed of transmission

Parameter 3– Incidence between animals and, when relevant, between animals and humans

Data on the incidence of SAV in ﬁsh have been described previously (see Section 1.2 Morbidity – Parameter 1).

There is no evidence of SAV transmission between animals and humans.

Parameter 4 – Transmission rate (beta) (from R₀ and infectious period) between animals and, when relevant, between animals and humans

Three studies reported relevant epidemiological characteristics: One study reported transmission rate for SAV and two studies reported basic reproduction number (Table6):

3.1.1.7. Article 7(a)(vii) The absence or presence and distribution of the disease in the union, and, where the disease is not present in the union, the risk of its introduction into the union

Presence and distribution

Parameter 1– Map where the disease is reported to be present in EU

The following map displays EU World Animal Health Information System (WOAH-WAHIS) data reﬂecting the epidemiological situation of SAV outbreaks as reported by veterinary authorities from Member States (MSs) (Figure1):

Table 6: Transmission rate (beta) and basic reproduction number (R₀) for infection with salmonid alphavirus

Country Indicator Study

population Value Reference

United Kingdom

Basic reproduction number PD

~1.0 Graham et al. (2006)

Norway Basic reproduction number PD

Range:1.0 and 2.9 Tavornpanich et al. (2013) Norway Transmission rate PD

(time unit = monthly)

Marine farmed salmonids

Range:~0 (September) to~3 (June)

Aldrin et al. (2015)

Figure 1: SAV outbreaks in Europe as reported by Veterinary Authorities to WOAH from 2018 to 2022; Source of the map: WOAH-WAHIS³

3https://wahis.woah.org/#/dashboards/country-or-disease-dashboard

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Parameter 2–Type of epidemiological occurrence (sporadic, epidemic, endemic) at MS level

Jansen et al. (2017) described the distribution of PD in Europe. The authors reported that 62% and 86% of salmonid sites in Ireland were affected by PD, in 2003 and 2004, respectively. In 2007, a large part of Western Norway became deﬁned as a SAV3 zone, where PD was considered endemic. Sporadic outbreaks of PD north of the endemic zones have been controlled up to 2017 by depopulation. Rodger and Mitchell (2007) reported that PD was endemic in most salmon marine sites in Ireland and in historically infected sites in other countries; and that the disease tended to recur in each successive generation of ﬁsh introduced onto the site irrespective of the duration of the fallowing period (McLoughlin and Graham, 2007).

Risk of introduction

Parameter 3– Routes of possible introduction

Not applicable. SAV has already been introduced in several EU countries.

Parameter 4– Number of animal moving and/or shipment size

Parameter 5– Duration of infectious period in animal and/or commodity Not applicable. SAV has already been introduced in several EU countries.

Parameter 6– List of control measures at border (testing, quarantine, etc.) Not applicable. SAV has already been introduced in several EU countries.

Parameter 7– Presence and duration of latent infection and/or carrier status.

Parameter 8– Risk of introduction by possible entry routes (considering parameters from 3 to 7) Not applicable. SAV has already been introduced in several EU countries.

3.1.1.8. Article 7(a)(viii) The existence of diagnostic and disease control tools Diagnostic tools

Parameter 1– Existence of diagnostic tools

A preliminary and indirect diagnosis can be based on gross clinical signs and histopathology, but because other pathogens may produce similar signs, the identification of viral molecules is required to confirm SAV infection (Karlsen and Johansen, 2017). The diagnosis of SAV is currently based on a combination of histopathological examination, antibody detection, virus culture and PCR technique (Deperasinska et al., 2018). The WOAH recommends the following: 1. Real-time RT-PCR for the surveillance of apparently healthy animals and for the presumptive diagnosis of clinically affected animals; and 2. amplicon sequencing for the confirmation of a suspect result from surveillance or presumptive diagnosis (WOAH, 2021).

Control tools

Parameter 2– Existence of control tools

Different tools, including biosecurity measures, vaccination, movement restrictions and selective breeding of resistant strains, are currently available in order to control SAV (Deperasinska et al., 2018).

The disease is managed as an endemic disease in Ireland and Scotland. It is managed as an endemic disease in western to mid-Norway, but in Northern parts of Norway, which are considered free of the disease, is treated as an exotic disease and emergency measures should be implemented.

In 2006, the regional industry established the ‘Hustadvika barrier’, a 15–20 km zone with no farming activities in mid-Norway, on the frontier between the endemic and non-endemic areas, with the purpose of preventing disease dissemination into the densely farmed areas further north in mid- Norway. Government regulations have been in place since 2007 requiring the depopulation of infected sites in disease-free areas and alterations to management practices in the endemic area (Pettersen et al., 2015b). In a new regulation from 2017, a PD endemic zone was deﬁned from Jæren in the south to the mid-Trøndelag. The areas south and north of this zone were deﬁned as PD-free

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surveillance zones (Norwegian Veterinary Institute, 2022). Mandatory screening of all seawater production sites was also introduced at this time. There has been a signiﬁcant decline in clinical SAV cases in the SAV3 endemic area at the west coast. The cause of this decline has yet to be investigated, but may be an effect of increased biosecurity measures, vaccination or a combination of these and other unknown factors (Sommerset et al., 2022).

Jansen et al. (2017) highlighted that, except for vaccination, there is currently very limited scientiﬁc knowledge regarding the impact of other management strategies for SAV, and the authors suggested further investigations be conducted.

3.1.2. Article 7(b) The impact of disease

3.1.2.1. Article 7(b)(i) The impact of the disease on agricultural and aquaculture production and other parts of the economy

The level of presence of the disease in the Union

Parameter 1– Number of MSs where the disease is present

The notiﬁcation and reporting of SAV is not mandatory at the EU level (cf. Article 5 of Regulation (EU) 2016/429). According to the European Union Reference Laboratory (EURL) for Fish and Crustacean Diseases,⁴between 2014 and 2021 SAV was detected in Austria, France, Germany, Ireland, Norway*, Poland, Serbia, Spain, Switzerland* and the United Kingdom (Scotland)*. As set out in Annexes I and II of the Commission Implementing Decision (EU)2021/260, the continental parts of Finland are currently regarded as being free of SAV.

*Not part of the European Union, but important considerations in the region.

The loss of production of the disease

Parameter 2 – Proportion of production losses (%) by epidemic/endemic situation (milk, growth, semen, meat, etc.)

Biomass lost through mortalities contributes to one part of the loss, but poor growth and a reduction inﬁllet quality are also major consequences of infection (Karlsen and Johansen, 2017).

A review of farm records from one of Scotland’s largest salmon producers revealed that from 2000 to 2009 PD accounted for the loss of 8.6% of total salmon biomass (Kilburn et al., 2012).

An 11.4% loss in growth over a 2-year period (2003 and 2004) has been associated with PD outbreaks in Ireland (Rodger and Mitchell, 2007).

Similarly, Norwegian field data have shown PD-affected fish groups have reduced growth rates compared to unaffected fish groups (Bang Jensen et al., 2012). In Norwegian SAV-infected Atlantic salmon farms, the production was reduced to 70% (P5:57% and P95:81%) of saleable biomass (Aunsmo et al., 2010).

A study concluded that the most important consequences of PD caused by SAV2 infection is reduced growth and feed conversion in large Atlantic salmon; the estimated impact corresponded to a growth reduction of 0.7 kg and 0.07 points increase in feed conversion ratio (Røsæg et al., 2019).

3.1.2.2. Article 7(b)(ii) The impact of the disease on human health Transmissibility between animals and humans

Parameter 1–Types of routes of transmission between animals and humans There is no evidence in the literature that SAV infects humans.

Parameter 2– Incidence of zoonotic cases

There is no evidence in the literature that SAV infects humans.

Transmissibility between humans

Parameter 3 – Human-to-human transmission is sufﬁcient to sustain sporadic cases or community-level outbreak

4https://www.eurl-ﬁsh-crustacean.eu/ﬁsh/survey-and-diagnosis

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Parameter 4– Sporadic, endemic, epidemic or pandemic potential.

Parameter 5– Disability-adjusted life year (DALY)

The availability of effective prevention or medical treatment in humans

Parameter 6 – Availability of medical treatment and their effectiveness (therapeutic effect and any resistance)

Parameter 7–Availability of vaccines and their effectiveness (reduced morbidity) There is no evidence in the literature that SAV infects humans.

3.1.2.3. Article 7(b)(iii) The impact of the disease on animal welfare

Parameter 1– Severity of clinical signs at case level and related level and duration of impairment The clinical progression of natural PD infection occurring in the seawater phase of the production cycle is typically characterised by three histologically distinct phases. The initial acute phase lasts for up to 10 days at 2–14°C, during which time infected ﬁsh may exhibit external signs such as lethargy, inappetence and production of yellow faecal casts due to lack of feeding. During this phase, inﬂammation in the pancreas and heart are also histologically detectable. The subacute phase lasts around 10–21 days from the onset of clinical signs and is characterised by histological lesions in pancreatic tissue, heart and skeletal muscle. Skeletal muscle lesions are the predominant histological feature observed in the chronic stages of infection, usually lasting for up to 42 days (Herath et al., 2017).

3.1.2.4. Article 7(b)(iv) The impact of the disease on biodiversity and the environment Biodiversity

Parameter 1– Endangered wild species affected: listed species as in CITES and/or IUCN list

The long rough dab, one of the species with incomplete evidence for susceptibility according to the WOAH (Section3.1.1.1Susceptible animal species) is listed as‘Endangered’in the IUCN list.

Parameter 2– Mortality in wild species

No information was found in the literature. However, in a Norwegian surveillance programme conducted among 453 wild Atlantic salmon and 100 wild sea trout caught in areas where SAV3 is endemic with frequent outbreaks of PD, only one released Atlantic salmon smolt tested positive for SAV3. In conclusion, it appears that while SAV is highly prevalent within the Norwegian aquaculture industry, it is found only at a low prevalence in wild brood ﬁsh (Biering et al., 2013). Similarly, no SAV antibodies were found in serum from wild salmonids in river systems in Northern Ireland, despite their proximity to SAV-infected aquaculture sites (Graham et al., 2003; Jansen et al., 2017). SAV infection seems to occur at low levels in wild salmonid and non-salmonid ﬁsh and there is no evidence that infections are associated with disease.

Environment

Parameter 3– Capacity of the pathogen to persist in the environment and cause mortality in wildlife As discussed previously (Section 3.1.1.5 Parameter 4 Persistence of the disease in an animal population or the environment), SAV may also survive in the environment such as in the water.

Nevertheless, it does not seem to cause mortality in wild susceptible species (Section 3.1.2.4 Parameter 2 mortality in wild species).

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3.1.3. Article 7(c) Its potential to generate a crisis situation and its potential use in bioterrorism

Parameter 1– Listed in WOAH/CFSPH classiﬁcation of pathogens

SAV is not listed by the Center for Food Security and Public Health (CFSPH).⁵ SAV is listed as a notiﬁable disease by WOAH.⁶

Parameter 2– Listed in the Encyclopaedia of Bioterrorism Defence of Australia Group SAV is not listed in the Encyclopaedia of Bioterrorism Defence of Australia Group.⁷ Parameter 3– Included in any other list of potential bio-agro-terrorism agents

SAV is not listed as a potential bio–agro-terrorism agent.

3.1.4. Article 7(d) The feasibility, availability and effectiveness of the following disease prevention and control measures

3.1.4.1. Article 7(d)(i) Diagnostic tools and capacities Availability

Parameter 1– Ofﬁcially/internationally recognised diagnostic tool, WOAH certiﬁed See Section3.1.1.8Diagnostic tools.

Effectiveness

Parameter 2– Sensitivity (Se) and Speciﬁcity (Sp) of diagnostic test

The sensitivity and speciﬁcity of the tests available for SAV diagnosis are described in Table 7 (WOAH, 2021).

Feasibility

Parameter 3–Type of sample matrix to be tested (blood, tissue, etc.)

The type of samples to be tested for SAV diagnostic are described in Table 8summarised from the WOAH (2021):

Table 7: Tests available for the diagnosis of SAV in Atlantic Salmon, and their reported sensitivity and speciﬁcity. Source: summarised from WOAH (2021)

Test Species Se Sp Reference

Real-time PCR Atlantic salmon 0.39 0.83 Hall et al. (2014), Jansen et al. (2019) 0.98 >0.99 Jansen et al. (2019)

Isolation of SAV in cell culture

Atlantic salmon 0.5 0.99 Hall et al. (2014), Jansen et al. (2019) 0.95 >0.99 Jansen et al. (2019)

Detection of neutralising activity against SAV

Atlantic salmon 0.085 0.74 Jansen et al. (2019) Histopathology Atlantic salmon 0.637 0.967 Jansen et al. (2019) Se: sensitivity; Sp: speciﬁcity.

Table 8: Types of tissues and samples to be tested for SAV diagnosis in Atlantic salmon. Source:

summarised from WOAH (2021)

Test Species Tissue or sample type Reference

Real-time PCR Atlantic salmon Kidney

Heart and mid-kidney

Hall et al. (2014), Jansen et al. (2019)

5https://www.cfsph.iastate.edu/diseaseinfo/

6https://www.woah.org/en/what-we-do/animal-health-and-welfare/animal-diseases/

7http://www.australiagroup.net/en/human_animal_pathogens.html

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3.1.4.2. Article 7(d)(ii) vaccination Availability

Parameter 1–Types of vaccines available on the market (live, inactivated, DIVA, etc.)

DNA-based and cell-culture-based virus-inactivated vaccines against PD in Atlantic salmon (Salmo salar) are both commercially available (WOAH, 2021). In 2017, the European Medicines Agency (EMA)⁸ issued a marketing authorisation for a DNA vaccine against PD in Atlantic salmon (CLYNAV^TM, Elanco GmbH) for all EU Countries. The commercially available vaccines in different countries in Europe found in the literature are provided in Table 9. Vaccines against SD in trout populations are not yet available.

Parameter 2–Availability/production capacity (per year)

No data were found in the literature about the availability and the production capacity of the vaccines.

Effectiveness

Parameter 3 – Field protection as reduced morbidity (as reduced susceptibility to infection and/or to disease)

The Norvax^® Compact PD vaccine demonstrated a reduction in mortality of at least 50% in vaccinated ﬁsh compared with unvaccinatedﬁsh at the same farm. Vaccination with Norvax^® Compact

Test Species Tissue or sample type Reference

Isolation of SAV in cell culture

Atlantic salmon Heart ventricle and head-kidney Hall et al. (2014), Jansen et al. (2019)

Detection of neutralising activity against SAV

Atlantic salmon Serum or plasma Jansen et al. (2019) Histopathology Atlantic salmon Heart and mid-kidney Jansen et al. (2019)

Table 9: Vaccines against PD in Atlantic salmon (Salmo salar) commercially available in Europe

Vaccine name Company Countries Type Administration Duration of protection ALPHA JECT^®

micro 1 PD

Pharmaq AS, (now part of Zoetis)

Ireland, Norway, UK

Inactivated SAV3 (strain ALV 405)

Intraperitoneal injection

At least 12 months AQUAVAC^®PD3

(Trivalent vaccine)

Intervet/MSD Animal Health Ireland (former Intervet)

Ireland, UK Inactivated for SAV1 (strain F93-125), IPNV and Aeromonas salmonicida

15 months

AQUAVAC^®PD7 (Heptavalent vaccine)

Intervet/MSD Animal Health

Norway Inactivated for SAV1 (strain F93-125), IPN,Aeromonas salmonicida, Aliivibrio salmonicida, Vibrio salmonicida, Vibrio anguillarum (O1, O2a), Moritella viscosa

At least 16 months

Norvax^® Compact PD

Intervet/MSD Animal Health (former Intervet)

Ireland, Norway, UK

Inactivated SAV1 (strain F93-125)

12–18 months

CLYNAV^TM Elanco GmbH Animal Health

EU (authorisation by EMA), Norway

Recombinant DNA plasmid of SAV3 virus

Intramuscular injection

9.5–12 months Bang Jensen et al. (2012), Deperasinska et al. (2018).

Summary of Product Characteristics (SPC): ALPHA JECT micro 1 PD (HPRA, 2015b), AQUAVAC^®PD3 (HPRA, 2015a), AQUAVAC^® PD7 (The Norwegian Medicines Agency, 2015), Norvax^®Compact PD:(HPRA, 2015a), CLYNAV^TM(EMA, 2017).

8European Medicines Agency:https://www.ema.europa.eu/en

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PD has been used in the Norwegian aquaculture of salmon since 2007, and has reduced the number of outbreaks in Norwegian salmon farms, the cumulative mortality and the number of discarded ﬁsh at slaughter as well as increased the growth rate compared to non-vaccinated farms (Bang Jensen et al., 2012; Deperasinska et al., 2018).

In two controlled field studies, the efficacy of three commercially SAV vaccines available in Norway was compared by measuring mortality and growth in farmed Atlantic salmon experiencing natural SAV2 and SAV3 outbreaks. Only the group immunised with the Clm6 vaccine (DNA-based vaccine CLYNAV^TM) provided protection against mortality compared with the control group, (reduction in mortality of 1.31% [CI 95: 0.8–1.8]). Significant protection against PD-induced loss of growth was similarly only found in the Clm6 group, with increased harvest weight estimated at 0.43 and 0.51 kg compared with the control group of the two controlledfield studies (Røsaeg et al., 2021).

In the context of a survey carried out in 2021 among fish health personnel and inspectors at the Norwegian Food Safety Authority, it was reported that of the respondents with experience with vaccination against PD (N = 43), approximately 50% stated that they have not observed PD disease after vaccination. A further 37% reported that there was less disease in vaccinated than in non- vaccinated fish. Some of the respondents linked this to vaccination with the DNA vaccine (Sommerset et al., 2022). In addition, vaccination results in reduced viral shedding from infected fish (Skjold et al., 2016; Sommerset et al., 2022).

Parameter 4– Duration of protection

According to the SPCs of the vaccines, the duration of immunity able to protect ﬁsh against SAV varies per vaccine: (i) at least 12 months for ALPHA JECT^® micro 1 PD vaccine, (ii) 15 months for AQUAVAC^® PD3, (iii) at least 16 months for AQUAVAC^® PD7, (iv) at least 12 months for reduction of heart lesions and 18 months for reduction of mortality and weight loss for Norvax^® Compact PD, (v) 1 year for reduction in impaired daily weight gain, and cardiac, pancreatic and skeletal muscle lesions and 9.5 months for reduction of mortality (demonstrated in a laboratory efﬁcacy study in saltwater conditions using a cohabitation challenge model) for CLYNAV^TM.

Feasibility

Parameter 5–Way of administration

Vaccines against SAV are usually administered by intraperitoneal injection (Gomez-Casado et al., 2011).

3.1.4.3. Article 7(d)(iii) Medical treatments Availability

Parameter 1–Types of drugs available on the market No effective treatment for SAV is currently available.

Parameter 2–Availability/production capacity (per year)

As currently there is no treatment available for SAV, Parameter 2 is not applicable for the assessment.

Parameter 3–Therapeutic effect in theﬁeld (effectiveness)

Feasibility

Parameter 4–Way of administration

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3.1.4.4. Article 7(d)(iv) Biosecurity measures Availability

Parameter 1–Available biosecurity measures

To avoid infection with SAV good husbandry practices are recommended, such as the use of appropriate sites for farming, segregation of generations, stocking with good quality fish, removal of dead fish, regular cleaning of tanks and pens and control of parasites and other pathogens, as well as careful handling of fish. Once an outbreak has started, mortality may be reduced by minimising handling and ceasing feeding (WOAH, 2021).

Ruane et al. (2008) recommended to maintain a high level of site biosecurity with emphasis on: (i) biosecurity measures for personnel, visitors and equipment, (ii) using a single bay management strategy, (iii) fast ﬁsh for 5–10 days on a pen-by-pen basis if pancreas disease is detected at an early stage and (iii) removing deadﬁsh from the pens frequently.

SAV is rapidly inactivated at pH 4 and pH 12, after heating 1 h to 60°C, as well as by UV light.

Commercially available disinfectants have been tested for efficacy against SAV under different conditions, all being found to be effective under at least some of the conditions tested (Graham et al., 2007a). Therefore, treatment and disposal of dead fish during an outbreak using the common practices of ensiling (low pH), alkaline hydrolysis (high pH) or composting (high temperatures) can effectively inactivate the virus (Ruane et al., 2008). Standard disinfection procedures are considered sufficient to prevent surface contamination of eggs by SAV (WOAH, 2021).

Proper boat and transporter cleaning and disinfection are also critical to control the spread of all infectious agents. The efﬁcient removal and safe disposal of dead ﬁsh may reduce the viral challenge.

Biosecure killing methods and safe disposal of offal and efﬂuent are also key to minimising the risk from these processes. Good sea lice control is desirable as sea lice may act as reservoirs or vectors of SAV even though there is no evidence that they can transmit SAV to the susceptible species (McLoughlin and Graham, 2007).

Fallowing of farm sites reduces or limits the build-up of SAV, a practice that is required in many countries (Jones et al., 2015).

Effectiveness

Parameter 2– Effectiveness of biosecurity measures in preventing the pathogen introduction

In 2007, the Norwegian aquaculture industry instigated the ‘PD-free’ project to control PD and reduce the losses through several mitigation measures including better utilisation of suitable sites, closure of poor sites, grouping sites with a single year class, etc. The project evaluation showed a 24% reduction in PD outbreaks in the ﬁrst 2 years of implementation (2007–2009), and a 10%

reduction of the overall losses from 2007 to 2010 (Jansen et al., 2017).

Feasibility

Parameter 3– Feasibility of biosecurity measure

Holdingfish while awaiting test results relies on having suitable biosecurity systems to hold the fish in a sustainable manner. Such systems must have sufficient space to hold the stock, have the ability to feed thefish and maintain the environmental quality of the water they are held in (Depner, 2017).

3.1.4.5. Article 7(d)(v) Restrictions on the movement of animals and products Availability

Parameter 1–Available movement restriction measures

Since 2007, restrictions have been applied in Norway for the movement of infectedfish to avoid the spread of SAV (Aslam et al., 2020). The Norwegian coastline is divided into one endemic and two non- endemic zones and SAV is notifiable in all zones. In the endemic zone, restrictions on the movement of fish are imposed on farms with either a suspicion or a confirmed diagnosis of SAV. In the non-endemic zones, SAV is as a general rule controlled by stamping-out farms with a confirmed diagnosis of SAV unless the risk of disease transmission is considered low (Bang Jensen et al., 2021).

Since 2014, SAV has been included in the list of infectious ﬁsh diseases at WOAH. As a consequence, countries that can document freedom from this disease are allowed to refuse to import salmonids from SAV-affected areas.

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Effectiveness

Parameter 2– Effectiveness of restriction of animal movement in preventing the between farm spread No information was found in the literature.

Feasibility

Parameter 3– Feasibility of restriction of animal movement No information was found in the literature.

3.1.4.6. Article 7(d)(vi) Killing of animals Availability

Parameter 1–Available methods for killing animals

Norway aims to control the spread of SAV beyond the endemic zones by depopulation. Sites within a 10 km radius of a depopulated site are sampled monthly over an extended period, deﬁned by the Norwegian Food Safety Authority, to ensure that no local spread occurs (Jansen et al., 2017).

As described in the Aquatic Code of the World Organisation for Animal Health (Chapters 7.3 and 7.4) (WOAH, 2022a,b) several killing methods exist, such as using an overdose of an anaesthetic agent or mechanical killing methods. The killing method should be selected taking into consideration ﬁsh welfare and biosecurity requirements, as well as the safety of the personnel. EFSA (2009) reported the following methods used for emergency killing: pharmacological, electrical and maceration. Broodstock is usually killed by the application of pharmacological methods before destruction.

Effectiveness

Parameter 2 – Effectiveness of killing animals (at farm level or within the farm) for reducing or stopping TH spread of the disease

A Norwegian study was conducted to evaluate the economic effects of different control strategies towards SAV in a PD-endemic area. In this study, a scenario where all farms were stamped out within 30 days of virus detection reduced the expected aggregated number of PD outbreaks from 162 to six.

A scenario where all farms were stamped out only after a clinical outbreak led to a reduction from 162 to 103 thus supporting the efﬁcacy of immediate measures (Pettersen et al., 2016; Bang Jensen et al., 2021).

Feasibility

Parameter 3– Feasibility of killing animals

Killing using an overdose of an anaesthetic (e.g. MS222) administered tofish kept in small volumes of water is the most feasible method available. Detailed protocols setting tank sizes and dosing per biomass of fish are not publicly available. Percussion stunning using a ‘priest’ followed by exsanguination or evisceration is most suitable for small numbers of fish. Electrical stunning is feasible if the appropriate equipment is available, but they are not widely used. Studies that address fish welfare before slaughter have concluded that many of the traditional systems used to stun fish including CO₂ narcosis are unacceptable as they cause avoidable stress before death. Exposure to water saturated with CO₂triggers aversive struggling and escape responses for several minutes before immobilisation, whereas in fish exposed to an electric current, immobilisation is close to instant (Gr€ans et al., 2016). A knowledge gap exists as there are no published data comparing rates of killing by different methods (Depner, 2017).

3.1.4.7. Article 7(d)(vii) Disposal of carcasses and other relevant animal by-products Availability

Parameter 1–Available disposal option

Assuming that deadfish shed SAV, then the prompt removal and safe disposal of dead animals is a simple husbandry measure that can help prevent the spread of disease. Measures will include the daily inspection of tanks and cages for evidence of dead or moribund fish and the use of systems for removing dead fish from fish farm tanks and cages and their safe disposal (e.g. by composting or ensiling).

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Carcasses fromﬁsh killed or found dead due to SAV infection belong to Category II materials and should be disposed of and destroyed according to the rules outlined in EC Regulation 1069/2009⁹and EC Regulation 142/2011¹⁰. The carcases and any relevant by-product must be transported in a sealed container, recorded on both arrival and departure of any site and should be disposed of and processed at an approved establishment. A list of premises approved by EU MSs can be found on the European Commission webpage.¹¹

Effectiveness

Parameter 2– Effectiveness of disposal options

As with other infectious diseases, the efﬁcient removal and safe disposal of carcasses and other animal by-products reduces the viral challenge. Biosecure killing methods and safe disposal of offal and efﬂuent are also key to minimising the risk from these processes (McLoughlin and Graham, 2007).

Feasibility

Parameter 3– Feasibility of disposal option

An alkaline hydrolysis method in which macerated fish are exposed to high pH (> 13) for 7 days inactivates high titres of virus and is recommended as a biosecurity treatment method for fish by- products that contain fish pathogens (Dixon et al., 2012). However, ensiling (a method of carcass disposal that involves lowering the pH to < 4) was determined as an infective method, in terms of biosecurity, for the disposal of dead fish (Smail et al., 1993; Dixon et al., 2012). Incineration or rendering is feasible where biosecurity measures can be implemented during the transport and an approved establishment is near the farm to process the carcasses (EFSA AHAW Panel, 2017b).

3.1.4.8. Article 7(d)(viii) Selective breeding; genetic resistance to infection Availability

Parameter 1–Available breeds resistant to the pathogen

Differences in susceptibility towards SAV among different family groups of Atlantic salmon have been observed in both challenge experiments and in the ﬁeld, indicating the potential for breeding for resistance (WOAH, 2021). Resistance to PD in Atlantic salmon has been shown to be moderate to highly heritable, with estimates ranging from 0.21 to 0.54 depending on the population used and the model of analysis applied (Norris et al., 2008; Gonen et al., 2015; Aslam et al., 2020).

Since the 1990s, Norwegian-owned Scotland farm has been involved in genetic improvement programmes aiming at targeting disease resistance traits in farmed salmon stocks in the United Kingdom and globally, including PD (Gonen et al., 2015; Regan et al., 2021). Commercial breeding programmes to increase resistance towards SAV are implemented in Ireland and Norway (WOAH, 2021).

Effectiveness

Parameter 2– Effectiveness of having resistant breeds

Breeding programmes in Ireland and Norway have successfully produced ﬁsh with increased resistance to disease caused by SAV (WOAH, 2021).

Feasibility

Parameter 3– Feasibility of having resistant breeds No information was found in the literature.

9Regulation (EC) No 1069/2009 of the European Parliament and of the Council of 21 October 2009 as amended:https://eur- lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A02009R1069-20191214

10 Commission Regulation (EU) No 142/2011 of 25 February 2011 as amended:https://eur-lex.europa.eu/legal-content/EN/TXT/?

uri=CELEX%3A02011R0142-20220417&qid=1686220344747

11 EC list of approved ABM establishments:https://food.ec.europa.eu/safety/animal-products/approved-establishments-abp_en

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